The cell biology of late blight disease

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Highlights

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The Phytophthora haustorium is a major site of secretion during infection.
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The host endocytic cycle contributes to biogenesis of the Extra-Haustorial Membrane.
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RXLR effectors manipulate host processes at diverse subcellular locations.
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They directly manipulate the activity or location of immune proteins.
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They also promote the activity of endogenous negative regulators of immunity.

Abstract

Late blight, caused by the oomycete Phytophthora infestans, is a major global disease of potato and tomato. Cell biology is teaching us much about the developmental stages associated with infection, especially the haustorium, which is a site of intimate interaction and molecular exchange between pathogen and host. Recent observations suggest a role for the plant endocytic cycle in specific recruitment of host proteins to the Extra-Haustorial Membrane, emphasising the unique nature of this membrane compartment. In addition, there has been a strong focus on the activities of RXLR effectors, which are delivered into plant cells to modulate and manipulate host processes. RXLR effectors interact directly with diverse plant proteins at a range of subcellular locations to promote disease.

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Most cited references 54

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A translocation signal for delivery of oomycete effector proteins into host plant cells.

Stephen C Whisson, Petra Boevink, Lucy N. Moleleki … (2007)

Bacterial, oomycete and fungal plant pathogens establish disease by translocation of effector proteins into host cells, where they may directly manipulate host innate immunity. In bacteria, translocation is through the type III secretion system, but analogous processes for effector delivery are uncharacterized in fungi and oomycetes. Here we report functional analyses of two motifs, RXLR and EER, present in translocated oomycete effectors. We use the Phytophthora infestans RXLR-EER-containing protein Avr3a as a reporter for translocation because it triggers RXLR-EER-independent hypersensitive cell death following recognition within plant cells that contain the R3a resistance protein. We show that Avr3a, with or without RXLR-EER motifs, is secreted from P. infestans biotrophic structures called haustoria, demonstrating that these motifs are not required for targeting to haustoria or for secretion. However, following replacement of Avr3a RXLR-EER motifs with alanine residues, singly or in combination, or with residues KMIK-DDK--representing a change that conserves physicochemical properties of the protein--P. infestans fails to deliver Avr3a or an Avr3a-GUS fusion protein into plant cells, demonstrating that these motifs are required for translocation. We show that RXLR-EER-encoding genes are transcriptionally upregulated during infection. Bioinformatic analysis identifies 425 potential genes encoding secreted RXLR-EER class proteins in the P. infestans genome. Identification of this class of proteins provides unparalleled opportunities to determine how oomycetes manipulate hosts to establish infection.

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Effector biology of plant-associated organisms: concepts and perspectives.

S Robatzek, K Belhaj, D Saunders … (2012)

Every plant is closely associated with a variety of living organisms. Therefore, deciphering how plants interact with mutualistic and parasitic organisms is essential for a comprehensive understanding of the biology of plants. The field of plant-biotic interactions has recently coalesced around an integrated model. Major classes of molecular players both from plants and their associated organisms have been revealed. These include cell surface and intracellular immune receptors of plants as well as apoplastic and host-cell-translocated (cytoplasmic) effectors of the invading organism. This article focuses on effectors, molecules secreted by plant-associated organisms that alter plant processes. Effectors have emerged as a central class of molecules in our integrated view of plant-microbe interactions. Their study has significantly contributed to advancing our knowledge of plant hormones, plant development, plant receptors, and epigenetics. Many pathogen effectors are extraordinary examples of biological innovation; they include some of the most remarkable proteins known to function inside plant cells. Here, we review some of the key concepts that have emerged from the study of the effectors of plant-associated organisms. In particular, we focus on how effectors function in plant tissues and discuss future perspectives in the field of effector biology.

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Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis

Tingli Liu, Tianqiao Song, Xiong Zhang … (2014)

Plant diseases caused by fungi and oomycetes pose an increasing threat to food security and ecosystem health worldwide. These filamentous pathogens, while taxonomically distinct, modulate host defense responses by secreting effectors, which are typically identified based on the presence of signal peptides. Here we show that Phytophthora sojae and Verticillium dahliae secrete isochorismatases (PsIsc1 and VdIsc1, respectively) that are required for full pathogenesis. PsIsc1 and VdIsc1 can suppress salicylate-mediated innate immunity in planta and hydrolyse isochorismate in vitro. A conserved triad of catalytic residues is essential for both functions. Thus, the two proteins are isochorismatase effectors that disrupt the plant salicylate metabolism pathway by suppressing its precursor. Furthermore, these proteins lack signal peptides, but exhibit characteristics that lead to unconventional secretion. Therefore, this secretion pathway is a novel mechanism for delivering effectors and might play an important role in host–pathogen interactions.

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Author and article information

Contributors

Paul RJ Birch

Journal

Journal ID (nlm-ta): Curr Opin Microbiol

Journal ID (iso-abbrev): Curr. Opin. Microbiol

Title: Current Opinion in Microbiology

Publisher: Current Biology

ISSN (Print): 1369-5274

ISSN (Electronic): 1879-0364

Publication date PMC-release: 1 December 2016

Publication date (Print): December 2016

Volume: 34

Pages: 127-135

Affiliations

[1 ]Cell and Molecular Sciences, James Hutton Institute, Errol Road, Invergowrie, Dundee DD2 5DA, UK

[2 ]Division of Plant Sciences, University of Dundee, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK

Article

Publisher ID: S1369-5274(16)30134-5

DOI: 10.1016/j.mib.2016.09.002

PMC ID: 5340842

PubMed ID: 27723513

SO-VID: cbe4c225-9e31-430e-9f7d-97e82a5dcf93

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This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

The cell biology of late blight disease

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The Biology of Macroalgae

Most cited references 54

A translocation signal for delivery of oomycete effector proteins into host plant cells.

Effector biology of plant-associated organisms: concepts and perspectives.

Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis

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